Aphid Alarm Pheromone: Isolation, Identification, Synthesis

Bowers, William S.; Nault, L. R.; Webb, R. E.; Dutky, S. R.

doi:10.1126/science.177.4054.1121

Cited by 284 publications

(162 citation statements)

References 3 publications

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“…EBF, a volatile sesquiterpene, is the major component of the aphid alarm pheromone [34]. Aphids secrete alarm pheromone from cornicles when attacked.…”

Section: Resultsmentioning

confidence: 99%

Parasitic wasp responses to symbiont-based defense in aphids

et al. 2012

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Background Recent findings indicate that several insect lineages receive protection against particular natural enemies through infection with heritable symbionts, but little is yet known about whether enemies are able to discriminate and respond to symbiont-based defense. The pea aphid, Acyrthosiphon pisum , receives protection against the parasitic wasp, Aphidius ervi , when infected with the bacterial symbiont Hamiltonella defensa and its associated bacteriophage APSE ( Acyrthosiphon pisum s econdary e ndosymbiont). Internally developing parasitoid wasps, such as A. ervi , use maternal and embryonic factors to create an environment suitable for developing wasps. If more than one parasitoid egg is deposited into a single aphid host (superparasitism), then additional complements of these factors may contribute to the successful development of the single parasitoid that emerges. Results We performed experiments to determine if superparasitism is a tactic allowing wasps to overcome symbiont-mediated defense. We found that the deposition of two eggs into symbiont-protected aphids significantly increased rates of successful parasitism relative to singly parasitized aphids. We then conducted behavioral assays to determine whether A. ervi selectively superparasitizes H. defensa -infected aphids. In choice tests, we found that A. ervi tends to deposit a single egg in uninfected aphids, but two or more eggs in H. defensa -infected aphids, indicating that oviposition choices may be largely determined by infection status. Finally, we identified differences in the quantity of the trans-β-farnesene, the major component of aphid alarm pheromone, between H. defensa -infected and uninfected aphids, which may form the basis for discrimination. Conclusions Here we show that the parasitic wasp A. ervi discriminates among symbiont-infected and uninfected aphids, and changes its oviposition behavior in a way that increases the likelihood of overcoming symbiont-based defense. More generally, our results indicate that natural enemies are not passive victims of defensive symbionts, and that an evolutionary arms race between A. pisum and the parasitoid A. ervi may be mediated by a bacterial symbiosis.

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“…EBF, a volatile sesquiterpene, is the major component of the aphid alarm pheromone [34]. Aphids secrete alarm pheromone from cornicles when attacked.…”

Section: Resultsmentioning

confidence: 99%

Parasitic wasp responses to symbiont-based defense in aphids

et al. 2012

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“…Alarm pheromone, which for most aphid species consists predominantly of EBF, is a central component of this intraspecies communication (1,2). Other alarm pheromone components have been studied less extensively, and it remains to be determined whether aphids can become habituated to these compounds.…”

Section: Discussionmentioning

confidence: 99%

“…Aphid avoidance of predators involves the production of an alarm pheromone. Across a remarkable diversity of aphids, the alarm pheromone contains a mixture of compounds with (E)-β-Farnesene (EBF) as the predominant component (1)(2)(3). Detection of EBF results in an array of aphid escape behaviors that, depending on the species and developmental stage, can include flying, walking away, and dropping off the plant.…”

mentioning

confidence: 99%

Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes

Vos

Cheng

Summers

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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In most aphid species, facultative parthenogenetic reproduction allows rapid growth and formation of large single-genotype colonies. Upon predator attack, individual aphids emit an alarm pheromone to warn the colony of this danger. (E)-β-farnesene (EBF) is the predominant constituent of the alarm pheromone in Myzus persicae (green peach aphid) and many other aphid species. Continuous exposure to alarm pheromone in aphid colonies raised on transgenic Arabidopsis thaliana plants that produce EBF leads to habituation within three generations. Whereas naive aphids are repelled by EBF, habituated aphids show no avoidance response. Similarly, individual aphids from the habituated colony can revert back to being EBF-sensitive in three generations, indicating that this behavioral change is not caused by a genetic mutation. Instead, DNA microarray experiments comparing gene expression in naive and habituated aphids treated with EBF demonstrate an almost complete desensitization in the transcriptional response to EBF. Furthermore, EBF-habituated aphids show increased progeny production relative to EBF-responsive aphids, with or without EBF treatment. Although both naive and habituated aphids emit EBF upon damage, EBF-responsive aphids have a higher survival rate in the presence of a coccinellid predator (Hippodamia convergens), and thus outperform habituated aphids that do not show an avoidance response. These results provide evidence that aphid perception of conspecific alarm pheromone aids in predator avoidance and thereby bestows fitness benefits in survivorship and fecundity. Therefore, although habituated M. persicae produce more progeny, EBF-emitting transgenic plants may have practical applications in agriculture as a result of increased predation of habituated aphids.aphid | (E)-beta-farnesene | Hippodamia convergens | microarray | sesquiterpene R apid population growth of aphids is facilitated by their parthenogenetic lifestyle, which often results in the establishment of large single-genotype colonies in the field. In agricultural settings, aphid populations can be controlled with natural enemies such as coccinellid beetles and parasitoid wasps. Despite the effectiveness of biological control, behavioral responses to the threat of predation may allow aphids to persist as pests. Aphid avoidance of predators involves the production of an alarm pheromone. Across a remarkable diversity of aphids, the alarm pheromone contains a mixture of compounds with (E)-β-Farnesene (EBF) as the predominant component (1-3). Detection of EBF results in an array of aphid escape behaviors that, depending on the species and developmental stage, can include flying, walking away, and dropping off the plant.EBF is a volatile sesquiterpene released from cornicles on the aphid's abdomen (4). When an aphid is attacked, it can release EBF in a range of concentrations, depending on the stress that is encountered, as well as the specific species, lineage, and developmental stage of the aphid itself (5-10). EBF-treated Acyrthosiphon pisum do no...

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“…The olfactory messages communicating the presence of a danger to the prey are the scents naturally released in the environment by the predators, named kairomones (4,5), and the alarm pheromones (APs) secreted by threatened or injured conspecifics (6)(7)(8)(9)(10)(11). Intraspecies communication by APs is an evolutionarily widespread phenomenon, presumably occurring in all animal phyla.…”

mentioning

confidence: 99%

Mouse alarm pheromone shares structural similarity with predator scents

Brechbühl

Moine

Klaey

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

162

234

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Sensing the chemical warnings present in the environment is essential for species survival. In mammals, this form of danger communication occurs via the release of natural predator scents that can involuntarily warn the prey or by the production of alarm pheromones by the stressed prey alerting its conspecifics. Although we previously identified the olfactory Grueneberg ganglion as the sensory organ through which mammalian alarm pheromones signal a threatening situation, the chemical nature of these cues remains elusive. We here identify, through chemical analysis in combination with a series of physiological and behavioral tests, the chemical structure of a mouse alarm pheromone. To successfully recognize the volatile cues that signal danger, we based our selection on their activation of the mouse olfactory Grueneberg ganglion and the concomitant display of innate fear reactions. Interestingly, we found that the chemical structure of the identified mouse alarm pheromone has similar features as the sulfur-containing volatiles that are released by predating carnivores. Our findings thus not only reveal a chemical Leitmotiv that underlies signaling of fear, but also point to a double role for the olfactory Grueneberg ganglion in intraspecies as well as interspecies communication of danger.olfaction | animal communication | behavior | calcium imaging

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Aphid Alarm Pheromone: Isolation, Identification, Synthesis

Abstract: A broadly interspecific aphid alarm pheromone was isolated from several economically important species of aphids and identified as trans-beta-farnesene.

Cited by 284 publications

References 3 publications

Parasitic wasp responses to symbiont-based defense in aphids

Parasitic wasp responses to symbiont-based defense in aphids

Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes

Mouse alarm pheromone shares structural similarity with predator scents

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